Summary of neuraminidase amino acid substitutions associated with reduced inhibition by neuraminidase inhibitors (NAI)*
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1 Summary of neuraminidase amino acid substitutions associated with reduced inhibition by neuraminidase inhibitors (NAI)* Susceptibility assessed by NA inhibition assays Source of Type/Subtype Amino acid N2 Comments substitution a numbering a (IC 50 fold change vs. wild type [NAI susceptible virus]) b viruses/ Reference Oseltamivir Zanamivir Peramivir Laninamivir Selection with c A(H1N1)pdm09 E119G 119 NI (3) HRI (832) RI (51)? d RG (52) Some IC 50 s were given for mixed virus populations; to be assessed using recombinant NA Only I427T affects IC 50?- to be assessed using recombinant NA E119V 119 RI (60) HRI (571) RI (25)? RG (52) D199G 198 RI (17) NI (6) NI (2)? RG (52) I223K 222 RI (12-39) NI (5-6) NI (1-4)? Sur (43) I223R 222 RI (28-45) RI (10-12)?? Clin/No; Clin/Ose/Zan; RG (17, 51, 63) I223V 222 NI (6) NI (2) NI (2)? RG (52) S247N 246 NI (4-8) NI (2-5) NI (1)? Sur (29) H275Y 274 HRI ( ) NI (1-6) RI/HRI (50-751) NI (1-2) Clin/Ose; Sur; In vitro (5, 12, 22, 32, 39, 45, 46, 48, 50, 60) N295S 294 HRI (208) NI (3) RI (12)? RG (52) D199N+H275Y HRI ( ) NI (2-3) HRI (108)? Clin/Ose (20, 50) I223K+H275Y HRI (>10822) RI (11) HRI (5343) RI (11) Sur; In vitro (46) I223R+H275Y HRI (>9100) RI (27-22) HRI (>7500) RI (17) Clin/Ose; RG (43, 46, 51) I223V+H275Y HRI (1733) NI (2) HRI (1331)? Clin/Ose; RG (10, 52) S247N+H275Y HRI (5880) NI (5) HRI (334)? Sur (29) Q313R+I427T RI (10-43) NI/RI (3-20) NI (4)? Sur (22, 25) A(H1N1) E119V 119 RI/HRI (15/1727) HRI (136/2144) HRI (5050)? RG (1, 11) Host cell- selected in both studies; not found in Q136K 136 NI (1) RI/HRI (36-327) RI (75-80)? Sur (27, 49) clinical specimens This result is virus specific Y155H 155 HRI (123) HRI (555)?? Sur (41) I223M 222 NI (8) NI (1) NI (1)? RG; In vitro/zan (26) I223V 222 NI (3) NI (2) NI (1)? RG; In vitro/zan (26) S247G 246 NI (5) NI (1)?? Sur (55) H275Y 274 HRI ( ) NI (1-2) HRI ( )? Sur; RG (11, 22, 40, 55) R293K 292 NI (1) RI (18?? RG (11) Last updated 21 October 2016 Page 1 of 9
2 Type/Subtype Comments Both changes were host cellselected Q136K was host cell-selected D151E/N was host cell-selected D151G was host cell-selected Q136K+D151N were host cellselected Susceptibility assessed by NA inhibition assays Source of Amino acid N2 substitution a numbering a (IC 50 fold change vs. wild type [NAI susceptible virus]) b viruses/ Reference Oseltamivir Zanamivir Peramivir Laninamivir Selection with c N295S 294 RI/HRI (40/197) NI (1/5) RI (12)? RG (1, 11) I117V+E119V NI (7) HRI (391)?? RG (11) I117M+E119V RI (20) HRI (181)?? RG (11) I117V+H275Y HRI (683) NI (1)?? RG (11) I117M+H275Y HRI (395) NI (1)?? RG (11) I117V+N295S RI (60) NI (1)?? RG (11) I117M+N295S RI (52) NI (4)?? RG (11) E119V+ H275Y RI (21) HRI (132)?? RG (11) Q136K+D151E NI (1) RI (25) RI (18)? Sur (49) Q136K+H275Y HRI (198) RI (15) HRI (1805)? Sur (49) D151E/N+H275Y HRI ( ) NI (1-3) RI/HRI (80-718)? Sur (49) D151G+H275Y HRI (1189) RI (14) HRI (1161)? Sur (49) I223M+H275Y HRI (1943) NI (1) HRI (400)? RG; In vitro/zan (26) I223V+H275Y HRI (584/971) NI (1/2) HRI (893)? RG; In vitro/zan (11, 26) I223V+N295S RI (97) NI (2)?? RG (11) R293K+H275Y HRI (207) NI (1)?? RG (11) N295S+H275Y HRI (108) NI (1)?? RG (11) S334N+H275Y HRI (415) NI (1)?? RG (11) I117V+N295S+H275Y HRI (336) RI (12)?? RG (11) I117M+N295S+H275Y HRI (121) RI (11)?? RG (11) Q136K+D151N+H275Y HRI (356) NI (4) HRI (23 00)? Sur (49) I223V+N295S+H275Y HRI (300) RI (13)?? RG (11) A(H5N1) V96A 116 RI (11-18) RI (10-63) NI (4)? Sur (6, 31) I97V 117 NI (5) NI (4)?? RG; Sur (33, 37) E99A 119 RI (35) HRI (1254)?? RG (33) E99G 119 NI (3-4) HRI ( ) RI/HRI (12-164)? RG; In vitro/zan (26) Q116L 136 RI (26) HRI (350)?? In vivo/zan (30) V129A 149 NI (4) NI (8)?? Sur (42) D179G 198 RI (32) RI (44) NI (4)? RG; In vitro/zan (26) I203M 222 RI (36) NI (1) NI (1)? RG; In vitro/zan (26) I203V 222 NI (7) NI (1) NI (1)? RG; In vitro/zan (26) Last updated 21 October 2016 Page 2 of 9
3 Type/Subtype Comments Susceptibility assessed by NA inhibition assays Source of Amino acid N2 substitution a numbering a (IC 50 fold change vs. wild type [NAI susceptible virus]) b viruses/ Oseltamivir Zanamivir Peramivir Laninamivir Selection with c Reference S227N 246 RI (24) NI (2)?? Sur (6) H255Y 274 HRI ( ) NI (1-3) HRI ( ) NI (6) Sur; Clin/Ose; RG; In vitro/zan (26, 33, 38, 44) N275S 294 RI/HRI (12-138) NI/RI (2-27) NI/RI/HRI (3-130)? Clin/Ose; RG (14, 33, 38) I97V+I294V RI (16) NI (1) NI (1)? Sur (31) I203M+H255Y HRI (8024) NI (3) HRI (3340)? RG; In vitro/zan (26) I203V+H255Y HRI (1925) NI (2) HRI (2106)? RG; In vitro/zan (26) K130N+I203L+S227N RI (77) NI (1)?? Sur (6) A(H3N2) E119D 119 NI (2) RI (32) NI (2)? RG (67) E119I 119 HRI (208) RI (17) NI (3)? Clin/Ose; In vitro (47) E119V 119 RI/HRI ( ) NI (1-7) NI (1-3) NI (3-4) Sur; Clin/Ose; In vitro; RG Host cell-selected, not found in clinical specimens T148I was host cell-selected (1, 34, 40, 47, 56, 61, 62, 67) Q136K 136 NI (1-7) RI/HRI (30-132)?? Sur (13, 48) D151E 151 RI (11) NI (2)?? RG (66) D151V/D 151 NI (8) HRI (164)?? Sur (55) I222L 222 NI (9) NI (2)?? RG (53) R224K 224 HRI (>4000) RI (>50)?? RG (66) Del e HRI ( ) NI (3) NI (1)? Clin/Ose (2) E276D 276 RI (15) HRI (160)?? RG (66) Clin/Ose; In (1, 8, 36, 55, 62, R292K 292 HRI (>10000) NI/RI/HRI (3-134) RI/HRI (14-719)? vitro/zan; RG 65-67) N294S 294 HRI ( ) NI (8) NI (1)? Clin/Ose; RG (1, 36) R371K 371 RI (45) RI (15)?? RG (66) E119V+T148I HRI (>6000) HRI (>800) HRI (>110) HRI (>250) Sur; In vitro; RG (61) E119V+I222L HRI (1571) RI (5)?? RG (53) E119V+I222V HRI ( ) NI (2) NI (7)? Clin/Ose (4, 56) A(H3N2)v S245N 245 NI (1) NI (1) NI (1) NI (1) Sur; RG (58) S247P 247 RI (42) HRI (266) NI (2) NI (9) Sur; RG (58) S245N+S247P RI (25-40) HI/HRI (66-235) NI (1-2) NI (7-9) Sur; RG (48, 58) A(H7N9) R289K 292 HRI (>4600) RI (11-64) HRI ( ) RI (15-33) In vitro; RG (23, 57) B E105K 110 NI (4-8) RI (15-42) HRI ( ) NI/RI (3-12) Clin/No; RG (19) Last updated 21 October 2016 Page 3 of 9
4 Type/Subtype Comments CDC: IC 50 s for a mixed virus population reported Susceptibility assessed by NA inhibition assays Source of Amino acid N2 substitution a numbering a (IC 50 fold change vs. wild type [NAI susceptible virus]) b viruses/ Reference Oseltamivir Zanamivir Peramivir Laninamivir Selection with c E117A 119 RI/HRI (3171) RI/HRI (12538) HRI (13780)? Sur; RG (7, 54) E117A or D 119 HRI (>300) HRI (>560) HRI (>1598)? RG (35) E117G 119 RI (31) RI/HRI (33-560) HRI (>1598)? In vitro; RG (3, 35) E117V 119 HRI (300) NI (2) HRI (531)? RG (35) Q138R 140 NI (1) RI (15) RI (41) RI (7) Sur; In vitro (18) P139S 141 RI (10) RI (25) HRI (322) RI (6) Sur; In vitro (18) G140R 142 RI (9) RI (30) HRI (321) RI (9) Sur; In vitro (18) R150K 152 HRI ( ) NI/RI/HRI (5-1000) HRI ( )? Clin; Clin/Zan; (21, 35, 40, 59, RG; Sur 66) D197E 198 RI (12-26) NI (3-7) RI (16-18)? Clin/No; Sur; RG (7, 28, 41) D197N 198 NI/RI (4-10) NI/RI (3-17) NI (5)? Clin/No; Clin/Ose; Sur (24, 34, 40, 55) D197Y 198 RI/HRI (15/57) RI (14) HRI (168)? Sur; RG (7, 16) A200A/T 201 RI (5-8) RI (5-7)?? Sur (48) I221L 222 HRI (70-121) RI (7-13)?? Clin/Ose (15) I221T 222 NI/RI (5-8) NI (2-4) RI (15-43) NI (<3) Clin/No; Sur; RG (24, 39, 41, 64){Burnham, 2014 #6313 I221V/I 222 NI (3-6) NI (1) NI (4-8)? Sur (59) A245T 246 RI (24) RI (39) RI (5) NI (3) Sur (39) H273Y 274 NI/RI (2-12) NI (1) RI/HRI (15-110)? Sur; RG (7, 50, 55) R292K 292 HRI (>300) RI (29) HRI (502)? RG (35) N294S 294 RI (17-61) NI (1-4) RI (31)? Clin/No; RG (7, 9) K360E f NI (2) NI (2) HRI (165) NI (<3) Sur (39) R374K 371 HRI (101/407) RI/HRI (29/145) HRI (352)? Sur; RG (7, 55) A395E 390 RI (5) NI (1) RI (5) NI (<3) Sur (39) G407S 402 NI (4) NI (7)?? Clin/Ose; Sur (24) D432G 429 NI (1) NI (1) RI (41) NI (<3) Sur (39) G140R+N144K NI (6) RI (10) HRI (257)? Sur (50) Y142H+G145R RI (5) NI (4) HRI (487) NI (<3) Sur (39) a Numbering is based on an alignment of neuraminidases from: A/Brisbane/59/2007 [H1N1], A/California/7/2009 [H1N1pdm09], A/turkey/Turkey/1/2005 [H5N1], A/Singapore/1/57 [H2N2], A/Perth/16/2009 [H3N2, A/Hong Kong/1074/97 [H9N2], A/Anhui/1/2013 [H7N9], A/Jiangxi-Donghu/346/2013 [H10N8], B/Brisbane/60/2008 [B/Vic lineage], B/Bangladesh/3333/2007 [B/Yam lineage]. Last updated 21 October 2016 Page 4 of 9
5 b Assessed by NA inhibition assays chemiluminescent (NA-Star), fluorescent (MUNANA), and/or colorimetric (fetuin). NAI phenotype is shown according to the referenced studies: NI, normal inhibition; RI, reduced inhibition; HRI, highly reduced inhibition as defined in - World Health Organization. Meetings of the WHO working group on surveillance of influenza antiviral susceptibility Geneva, November 2011 and June Wkly Epidemiol Rec Sep 28;87(39): c Source: Sur, surveillance studies; Clin, clinical detection; RG, reverse genetics; In vitro, cell-culture studies; In vivo, animal studies. Drug use: No, no NAI used; Ose, oseltamivir; Zan, zanamivir. d? indicates that the NAI(s) indicated were not studied. e Del indicated deletion of the three amino acids indicated. f Precise N2 numbering cannot be given as the influenza B NA carries an insertion in the alignment compared to the H3N2 NA. * Substitutions table developed by the WHO GISRS antiviral susceptibility expert working group (AVWG) Last updated 21 October 2016 Page 5 of 9
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8 36. Kiso, M., K. Mitamura, Y. Sakai-Tagawa, K. Shiraishi, C. Kawakami, K. Kimura, F. G. Hayden, N. Sugaya, and Y. Kawaoka Resistant influenza A viruses in children treated with oseltamivir: descriptive study. Lancet 364: Le, M. T., H. F. Wertheim, H. D. Nguyen, W. Taylor, P. V. Hoang, C. D. Vuong, H. L. Nguyen, H. H. Nguyen, T. Q. Nguyen, T. V. Nguyen, T. D. Van, B. T. Ngoc, T. N. Bui, B. G. Nguyen, L. T. Nguyen, S. T. Luong, P. H. Phan, H. V. Pham, T. Nguyen, A. Fox, C. V. Nguyen, H. Q. Do, M. Crusat, J. Farrar, H. T. Nguyen, M. D. de Jong, and P. Horby Influenza A H5N1 clade virus with a different antiviral susceptibility profile replaced clade 1 virus in humans in northern Vietnam. PloS one 3:e Le, Q. M., M. Kiso, K. Someya, Y. T. Sakai, T. H. Nguyen, K. H. Nguyen, N. D. Pham, H. H. Ngyen, S. Yamada, Y. Muramoto, T. Horimoto, A. Takada, H. Goto, T. Suzuki, Y. Suzuki, and Y. Kawaoka Avian flu: isolation of drug-resistant H5N1 virus. Nature 437: Leang, S. K., S. Kwok, S. G. Sullivan, S. Maurer-Stroh, A. Kelso, I. G. Barr, and A. C. Hurt Peramivir and laninamivir susceptibility of circulating influenza A and B viruses. Influenza and other respiratory viruses 8: Mishin, V. P., F. G. Hayden, and L. V. Gubareva Susceptibilities of antiviral-resistant influenza viruses to novel neuraminidase inhibitors. Antimicrobial agents and chemotherapy 49: Monto, A. S., J. L. McKimm-Breschkin, C. Macken, A. W. Hampson, A. Hay, A. Klimov, M. Tashiro, R. G. Webster, M. Aymard, F. G. Hayden, and M. Zambon Detection of influenza viruses resistant to neuraminidase inhibitors in global surveillance during the first 3 years of their use. Antimicrobial agents and chemotherapy 50: Naughtin, M., J. C. Dyason, S. Mardy, S. Sorn, M. von Itzstein, and P. Buchy Neuraminidase inhibitor sensitivity and receptor-binding specificity of Cambodian clade 1 highly pathogenic H5N1 influenza virus. Antimicrobial agents and chemotherapy 55: Nguyen, H. T., A. M. Fry, P. A. Loveless, A. I. Klimov, and L. V. Gubareva Recovery of a multidrug-resistant strain of pandemic influenza A 2009 (H1N1) virus carrying a dual H275Y/I223R mutation from a child after prolonged treatment with oseltamivir. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America 51: Nguyen, H. T., T. Nguyen, V. P. Mishin, K. Sleeman, A. Balish, J. Jones, A. Creanga, H. Marjuki, T. M. Uyeki, D. H. Nguyen, D. T. Nguyen, H. T. Do, A. I. Klimov, C. T. Davis, and L. V. Gubareva Antiviral susceptibility of highly pathogenic avian influenza A(H5N1) viruses isolated from poultry, Vietnam, Emerging infectious diseases 19: Nguyen, H. T., T. G. Sheu, V. P. Mishin, A. I. Klimov, and L. V. Gubareva Assessment of pandemic and seasonal influenza A (H1N1) virus susceptibility to neuraminidase inhibitors in three enzyme activity inhibition assays. Antimicrobial agents and chemotherapy 54: Nguyen, H. T., A. A. Trujillo, T. G. Sheu, M. Levine, V. P. Mishin, M. Shaw, E. W. Ades, A. I. Klimov, A. M. Fry, and L. V. Gubareva Analysis of influenza viruses from patients clinically suspected of infection with an oseltamivir resistant virus during the 2009 pandemic in the United States. Antiviral research 93: Okomo-Adhiambo, M., G. J. Demmler-Harrison, V. M. Deyde, T. G. Sheu, X. Xu, A. I. Klimov, and L. V. Gubareva Detection of E119V and E119I mutations in influenza A (H3N2) viruses isolated from an immunocompromised patient: challenges in diagnosis of oseltamivir resistance. Antimicrobial agents and chemotherapy 54: Okomo-Adhiambo, M., H. T. Nguyen, A. Abd Elal, K. Sleeman, A. M. Fry, and L. V. Gubareva Drug susceptibility surveillance of influenza viruses circulating in the United States in : application of the WHO antiviral working group criteria. Influenza and other respiratory viruses 8: Okomo-Adhiambo, M., H. T. Nguyen, K. Sleeman, T. G. Sheu, V. M. Deyde, R. J. Garten, X. Xu, M. W. Shaw, A. I. Klimov, and L. V. Gubareva Host cell selection of influenza neuraminidase variants: implications for drug resistance monitoring in A(H1N1) viruses. Antiviral research 85: Okomo-Adhiambo, M., K. Sleeman, C. Lysen, H. T. Nguyen, X. Xu, Y. Li, A. I. Klimov, and L. V. Gubareva Neuraminidase inhibitor susceptibility surveillance of influenza viruses circulating worldwide during the 2011 Southern Hemisphere season. Influenza and other respiratory viruses 7: Pizzorno, A., Y. Abed, X. Bouhy, E. Beaulieu, C. Mallett, R. Russell, and G. Boivin Impact of mutations at residue I223 of the neuraminidase protein on the resistance profile, replication level, and virulence of the 2009 pandemic influenza virus. Antimicrobial agents and chemotherapy 56: Pizzorno, A., X. Bouhy, Y. Abed, and G. Boivin Generation and characterization of recombinant pandemic influenza A(H1N1) viruses resistant to neuraminidase inhibitors. The Journal of infectious diseases 203: Last updated 21 October 2016 Page 8 of 9
9 53. Richard, M., O. Ferraris, A. Erny, M. Barthelemy, A. Traversier, M. Sabatier, A. Hay, Y. P. Lin, R. J. Russell, and B. Lina Combinatorial effect of two framework mutations (E119V and I222L) in the neuraminidase active site of H3N2 influenza virus on resistance to oseltamivir. Antimicrobial agents and chemotherapy 55: Sheu, T. G., V. M. Deyde, R. J. Garten, A. I. Klimov, and L. V. Gubareva Detection of antiviral resistance and genetic lineage markers in influenza B virus neuraminidase using pyrosequencing. Antiviral research 85: Sheu, T. G., V. M. Deyde, M. Okomo-Adhiambo, R. J. Garten, X. Xu, R. A. Bright, E. N. Butler, T. R. Wallis, A. I. Klimov, and L. V. Gubareva Surveillance for neuraminidase inhibitor resistance among human influenza A and B viruses circulating worldwide from 2004 to Antimicrobial agents and chemotherapy 52: Simon, P., B. P. Holder, X. Bouhy, Y. Abed, C. A. Beauchemin, and G. Boivin The I222V neuraminidase mutation has a compensatory role in replication of an oseltamivir-resistant influenza virus A/H3N2 E119V mutant. Journal of clinical microbiology 49: Sleeman, K., Z. Guo, J. Barnes, M. Shaw, J. Stevens, and L. V. Gubareva R292K substitution and drug susceptibility of influenza A(H7N9) viruses. Emerging infectious diseases 19: Sleeman, K., V. P. Mishin, Z. Guo, R. J. Garten, A. Balish, A. M. Fry, J. Villanueva, J. Stevens, and L. V. Gubareva Antiviral susceptibility of variant influenza A(H3N2)v viruses isolated in the United States from 2011 to Antimicrobial agents and chemotherapy 58: Sleeman, K., T. G. Sheu, Z. Moore, S. Kilpatrick, S. Garg, A. M. Fry, and L. V. Gubareva Influenza B viruses with mutation in the neuraminidase active site, North Carolina, USA, Emerging infectious diseases 17: Takashita, E., S. Fujisaki, N. Kishida, H. Xu, M. Imai, M. Tashiro, T. Odagiri, and J. Influenza Virus Surveillance Group of Characterization of neuraminidase inhibitor-resistant influenza A(H1N1)pdm09 viruses isolated in four seasons during pandemic and post-pandemic periods in Japan. Influenza and other respiratory viruses 7: Tamura, D., H. T. Nguyen, K. Sleeman, M. Levine, V. P. Mishin, H. Yang, Z. Guo, M. Okomo-Adhiambo, X. Xu, J. Stevens, and L. V. Gubareva Cell culture-selected substitutions in influenza A(H3N2) neuraminidase affect drug susceptibility assessment. Antimicrobial agents and chemotherapy 57: Tamura, D., N. Sugaya, M. Ozawa, R. Takano, M. Ichikawa, M. Yamazaki, C. Kawakami, H. Shimizu, R. Uehara, M. Kiso, E. Kawakami, K. Mitamura, and Y. Kawaoka Frequency of drug-resistant viruses and virus shedding in pediatric influenza patients treated with neuraminidase inhibitors. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America 52: van der Vries, E., F. F. Stelma, and C. A. Boucher Emergence of a multidrug-resistant pandemic influenza A (H1N1) virus. The New England journal of medicine 363: Wang, D., K. Sleeman, W. Huang, H. T. Nguyen, M. Levine, Y. Cheng, X. Li, M. Tan, X. Xing, X. Xu, A. I. Klimov, L. V. Gubareva, and Y. Shu Neuraminidase inhibitor susceptibility testing of influenza type B viruses in China during 2010 and 2011 identifies viruses with reduced susceptibility to oseltamivir and zanamivir. Antiviral research 97: Yen, H. L., L. M. Herlocher, E. Hoffmann, M. N. Matrosovich, A. S. Monto, R. G. Webster, and E. A. Govorkova Neuraminidase inhibitor-resistant influenza viruses may differ substantially in fitness and transmissibility. Antimicrobial agents and chemotherapy 49: Yen, H. L., E. Hoffmann, G. Taylor, C. Scholtissek, A. S. Monto, R. G. Webster, and E. A. Govorkova Importance of neuraminidase active-site residues to the neuraminidase inhibitor resistance of influenza viruses. Journal of virology 80: Zurcher, T., P. J. Yates, J. Daly, A. Sahasrabudhe, M. Walters, L. Dash, M. Tisdale, and J. L. McKimm-Breschkin Mutations conferring zanamivir resistance in human influenza virus N2 neuraminidases compromise virus fitness and are not stably maintained in vitro. The Journal of antimicrobial chemotherapy 58: Last updated 21 October 2016 Page 9 of 9
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